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The Effects of Aging on Testicular Volume and Glucose Metabolism: an Investigation with Ultrasonography and FDG-PET

Abstract

Objectives

To investigate the effects of senescence on testicular volume and metabolism by quantitative analysis of volumetric and functional data provided by genital ultrasonography (US) and 2-deoxy-2-[18F]fluoro-D-glucosepositron emission tomography (FDG-PET), respectively.

Methods

Three hundred twenty (PET 173, US 147) male subjects (average age, 47.9 ± 24.1 years; range, 11–90 years) who previously underwent US or FDG-PET imaging were included in this retrospective study. Testicular volumes and FDG maximum standardized uptake values (SUVmax) were correlated with age using polynomial regression and Pearson linear regression analysis.

Results

With cross-sectional analysis, the best-fit curves demonstrated statistically significant overall correlations between changes in both the volume and metabolism (SUVmax) of the testicle and increasing age (volume: R 2 = 0.42, p = 0.0002; SUVmax: R 2 = 0.26, p < 0.0001). Testicular volume rapidly increases during puberty and peaks at age 30 years. Subsequently, the volume of the testes stabilizes in a plateau-like manner until age 60 years. After age 60 years, this study shows that testicular volume decreases significantly. Testicular glucose metabolism increases until age 40 years, after which it declines gradually over time at a constant rate.

Conclusion

Testicular volume and metabolism appear to be significantly affected by advancing age at different rates during the different stages of lifespan. The rapid increase in testicular volume and metabolism parallel the onset and progression of puberty and positively correlate with increasing age up to ages 30–40 years. Between ages 40 and 60 years, testicular volume and metabolism remain relatively constant with only a minimal decline. After age of 60 years, the testicular volume significantly declines, while testicular metabolism progressively declines until age 90 years.

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References

  1. Wehrli NE, Bural G, Houseni M, Alkhawaldeh K, Alavi A, Torigian DA (2007) Determination of age-related changes in structure and function of skin, adipose tissue, and skeletal muscle with computed tomography, magnetic resonance imaging, and positron emission tomography. Semin Nucl Med 37(3):195–205

    PubMed  Article  Google Scholar 

  2. Well D, Yang H, Houseni M, Iruvuri S, Alzeair S, Sansovini M, Wintering N, Alavi A, Torigian DA (2007) Age-related structural and metabolic changes in the pelvic reproductive end organs. Semin Nucl Med 37(3):173–184

    PubMed  Article  Google Scholar 

  3. Dreher JC, Meyer-Lindenberg A, Kohn P, Berman KF (2008) Age-related changes in midbrain dopaminergic regulation of the human reward system. Proc Natl Acad Sci USA 105(39):15106–15111

    PubMed  Article  CAS  Google Scholar 

  4. Fan C, Hernandez-Pampaloni M, Houseni M, Chamroonrat W, Basu S, Kumar R, Dadparvar S, Torigian DA, Alavi A (2007) Age-related changes in the metabolic activity and distribution of the red marrow as demonstrated by 2-deoxy-2-[F-18] fluoro-d-glucose-positron emission tomography. Mol Imaging Biol 9(5):300–307

    PubMed  Article  Google Scholar 

  5. Kochunov P, Ramage AE, Lancaster JL, Robin DA, Narayana S, Coyle T, Royall DR, Fox P (2009) Loss of cerebral white matter structural integrity tracks the gray matter metabolic decline in normal aging. Neuroimage 45(1):17–28

    PubMed  Article  CAS  Google Scholar 

  6. Vermeulen A, Kaufman JM (1995) Ageing of the hypothalamo-pituitary-testicular axis in men. Horm Res 43(1-3):25–28, Review

    PubMed  Article  CAS  Google Scholar 

  7. Casulari LA, da Motta LD (2008) Diagnostic of andropause: a problem not yet solved. Arq Bras Endocrinol Metabol 52(9):1401–1402

    PubMed  Google Scholar 

  8. Kitajima K, Nakamoto Y, Senda M, Onishi Y, Okizuka H, Sugimura K (2007) Normal uptake of 18F-FDG in the testis: an assessment by PET/CT. Ann Nucl Med 21(7):405–410

    PubMed  Article  Google Scholar 

  9. Kosuda S, Fisher S, Kison PV, Wahl RL, Grossman HB (1997) Uptake of 2-deoxy-2-[18F]fluoro-D-glucose in the normal testis: retrospective PET study and animal experiment. Ann Nucl Med 11(3):195–199

    PubMed  Article  CAS  Google Scholar 

  10. Zachmann M, Prader A, Kind HP, Häfliger H, Budliger H (1974) Testicular volume during adolescence. Cross-sectional and longitudinal studies. Helv Paediatr Acta 29(1):61–72

    PubMed  CAS  Google Scholar 

  11. Santiemma V, Rosati P, Guerzoni C, Mariani S, Beligotti F, Magnanti M, Garufi G, Galoni T, Fabbrini A (1992) Human Sertoli cells in vitro: morphological features and androgen-binding protein secretion. J Steroid Biochem Mol Biol 43(5):423–429

    PubMed  Article  CAS  Google Scholar 

  12. Chen YI, Payne AH, Kelch RP (1976) FSH stimulation of Leydig cell function in the hypophysectomized immature rat. Proc Soc Exp Biol Med 153:473–47

    PubMed  CAS  Google Scholar 

  13. Van Burden WMO, Roodnat B, de Jong FH, Mulder E, van der Molen HJ (1976) Hormonal regulation of LH stimulation of testosterone production in isolated Leydig cells of immature rats: the effect of hypophysectomy. FSH and estradiol-17ß. Steroids 28:847–866

    Article  Google Scholar 

  14. Noorafshan A, Karbalay-Doust S, Ardekani FM (2005) High doses of nandrolone decanoate reduce volume of testis and length of seminiferous tubules in rats. APMIS 113(2):122–125

    PubMed  Article  CAS  Google Scholar 

  15. Kothari LK, Gupta AS (1974) Effect of ageing on the volume, structure and total Leydig cell content of the human testis. Int J Fertil 19(3):140–146

    PubMed  CAS  Google Scholar 

  16. Mahmoud AM, Goemaere S, El-Garem Y, Van Pottelbergh I, Comhaire FH, Kaufman JM (2003) Testicular volume in relation to hormonal indices of gonadal function in community-dwelling elderly men. J Clin Endocrinol Metab 88(1):179–184

    PubMed  Article  CAS  Google Scholar 

  17. Wu CY, Yu TJ, Chen MJ (2000) Age related testosterone level changes and male andropause syndrome. Chang Gung Med J 23(6):348–353

    PubMed  CAS  Google Scholar 

  18. Harman SM, Tsitouras PD (1980) Reproductive hormones in aging men. I. Measurement of sex steroids, basal luteinizing hormone, and Leydig cell response to human chorionic gonadotropin. J Clin Endocrinol Metab 51(1):35–40

    PubMed  Article  CAS  Google Scholar 

  19. Feldman HA, Longcope C, Derby CA, Johannes CB, Araujo AB, Coviello AD, Bremner WJ, McKinlay JB (2002) Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts male aging study. J Clin Endocrinol Metab 87(2):589–598

    PubMed  Article  CAS  Google Scholar 

  20. Midzak AS, Chen H, Papadopoulos V, Zirkin BR (2009) Leydig cell aging and the mechanisms of reduced testosterone synthesis. Mol Cell Endocrinol 299(1):23–31

    PubMed  Article  CAS  Google Scholar 

  21. Hermann M, Untergasser G, Rumpold H, Berger P (2000) Aging of the male reproductive system. Exp Gerontol 35(9-10):1267–1279, Review

    PubMed  Article  CAS  Google Scholar 

  22. Hermann M, Berger P (2001) Hormonal changes in aging men: a therapeutic indication? Exp Gerontol 36(7):1075–1082, Review

    PubMed  Article  CAS  Google Scholar 

  23. Labrie F, Bélanger A, Cusan L, Gomez JL, Candas B (1997) Marked decline in serum concentrations of adrenal C19 sex steroid precursors and conjugated androgen metabolites during aging. J Clin Endocrinol Metab 82(8):2396–2402

    PubMed  Article  CAS  Google Scholar 

  24. Rudman D, Kutner MH, Rogers CM, Lubin MF, Fleming GA, Bain RP (1981) Impaired growth hormone secretion in the adult population: relation to age and adiposity. J Clin Invest 67(5):1361–1369

    PubMed  Article  CAS  Google Scholar 

  25. Madersbacher S, Stulnig T, Huber LA, Schönitzer D, Dirnhofer S, Wick G, Berger P (1993) Serum glycoprotein hormones and their free alpha-subunit in a healthy elderly population selected according to the SENIEUR protocol. Analyses with ultrasensitive time resolved fluoroimmunoassays. Mech Ageing Dev 71(3):223–233

    PubMed  Article  CAS  Google Scholar 

  26. Gray A, Feldman HA, McKinlay JB, Longcope C (1991) Age, disease, and changing sex hormone levels in middle-aged men: results of the Massachusetts Male Aging Study. J Clin Endocrinol Metab 73:1016–1025

    PubMed  Article  CAS  Google Scholar 

  27. Veldhuis JD, Bae A, Swerdloff RS, Iranmanesh A, Wang C (2005) Experimentally induced androgen depletion accentuates ethnicity-related contrasts in luteinizing hormone secretion in Asian and Caucasian men. J Clin Endocrinol Metab 90(3):1632–1638

    PubMed  Article  CAS  Google Scholar 

  28. Neaves WB, Johnson L, Porter JC, Parker CR Jr, Petty CS (1984) Leydig cell numbers, daily sperm production, and serum gonadotropin levels in aging men. J Clin Endocrinol Metab 59(4):756–763

    PubMed  Article  CAS  Google Scholar 

  29. Nieschlag E, Lammers U, Freischem CW, Langer K, Wickings EJ (1982) Reproductive functions in young fathers and grandfathers. J Clin Endocrinol Metab 55(4):676–681

    PubMed  Article  CAS  Google Scholar 

  30. Kaufman JM, Vermeulen A (1997) Declining gonadal function in elderly men. Baillières Clin Endocrinol Metab 11(2):289–309

    PubMed  Article  CAS  Google Scholar 

  31. Christ-Crain M, Mueller B, Gasser TC, Kraenzlin M, Trummler M, Huber P, Meier C (2004) Is there a clinical relevance of partial androgen deficiency of the aging male? J Urol 172(2):624–627

    PubMed  Article  CAS  Google Scholar 

  32. Elmlinger MW, Kühnel W, Döller PC (2006) Evaluation of direct and indirect markers to assess the androgen status in healthy males during aging. Clin Lab 52(9–10):491–496

    PubMed  CAS  Google Scholar 

  33. Tenover JS, Matsumoto AM, Plymate SR, Bremner WJ (1987) The effects of aging in normal men on bioavailable testosterone and luteinizing hormone secretion: response to clomiphene citrate. J Clin Endocrinol Metab 65(6):1118–1126

    PubMed  Article  CAS  Google Scholar 

  34. Veldhuis JD, Keenan DM, Iranmanesh A (2005) Mechanisms of ensemble failure of the male gonadal axis in aging. J Endocrinol Investig 28(3 Suppl):8–13

    CAS  Google Scholar 

  35. Furlan PM, Rosso C, Rolle L, Fontana D (1993) Intervention models in andrology in adult–elderly patients with psychogenic erectile dysfunction. Arch Ital Urol Androl 65(5):523–528

    PubMed  CAS  Google Scholar 

  36. Sternbach H (1998) Age-associated testosterone decline in men: clinical issues for psychiatry. Am J Psychiatry 155(10):1310–1318

    PubMed  CAS  Google Scholar 

  37. Seftel A (2002) Memory loss as reported symptom of andropause. J Urol 168:862

    Google Scholar 

  38. Morley JE (2000) Andropause, testosterone therapy, and quality of life in aging men. Cleve Clin J Med 67(12):880–882

    PubMed  CAS  Google Scholar 

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Correspondence to Abass Alavi.

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Yang, H., Chryssikos, T., Houseni, M. et al. The Effects of Aging on Testicular Volume and Glucose Metabolism: an Investigation with Ultrasonography and FDG-PET. Mol Imaging Biol 13, 391–398 (2011). https://doi.org/10.1007/s11307-010-0341-x

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  • DOI: https://doi.org/10.1007/s11307-010-0341-x

Key words

  • Aging
  • Andropause
  • Testis
  • Male hypogonadism
  • Endocrinology
  • Ultrasonography
  • Positron emission tomography